Boosting γδ T cell-mediated antibody-dependent cellular cytotoxicity by PD-1 blockade in follicular lymphoma

References

• Huet S, Sujobert P, Salles G. From genetics to the clinic: a translational perspective on follicular lymphoma. Nat Rev Cancer. 2018;18(4):224–239. doi:10.1038/nrc.2017.127.
   PubMed Web of Science ®Google Scholar
• Horning SJ, Rosenberg SA. The natural history of initially untreated low-grade non-Hodgkin’s lymphomas. N Engl J Med. 1984 Dec 6;311(23):1471–1475. doi:10.1056/NEJM198412063112303.
   PubMed Web of Science ®Google Scholar
• de Jong D. Molecular pathogenesis of follicular lymphoma: a cross talk of genetic and immunologic factors. J Clin Oncol. 2005;23(26):6358–6363. doi:10.1200/JCO.2005.26.856.
   PubMed Web of Science ®Google Scholar
• Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, Fisher RI, Braziel RM, Rimsza LM, Grogan TM, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med.2004;351(21):2159–2169. doi:10.1056/NEJMoa041869.
   PubMed Web of Science ®Google Scholar
• Tosolini M, Algans C, Pont F, Ycart B, Fournié JJ. Large-scale microarray profiling reveals four stages of immune escape in non-Hodgkin lymphomas. Oncoimmunol. 2016;5(7):e1188246. doi:10.1080/2162402X.2016.1188246.
   PubMed Web of Science ®Google Scholar
• Laurent C, Charmpi K, Gravelle P, Tosolini M, Franchet C, Ysebaert L, Brousset P, Bidaut A, Ycart B, Fournié JJ. Several immune escape patterns in non-Hodgkin’s lymphomas. Oncoimmunol. 2015;4(8):e1026530. doi:10.1080/2162402X.2015.1026530.
   PubMed Web of Science ®Google Scholar
• Gravelle P, Burroni B, Péricart S, Rossi C, Bezombes C, Tosolini M, Damotte D, Brousset P, Fournié JJ, Laurent C. Mechanisms of PD-1/PD-L1 expression and prognostic relevance in non-Hodgkin lymphoma: a summary of immunohistochemical studies. Oncotarget. 2017;8(27):44960–44975. doi:10.18632/oncotarget.16680.
   PubMedGoogle Scholar
• Goodman A, Patel SP, Kurzrock R. PD-1-PD-L1 immune-checkpoint blockade in B-cell lymphomas. Nat Rev Clin Oncol. 2017;14(4):203–220. doi:10.1038/nrclinonc.2016.168.
   PubMed Web of Science ®Google Scholar
• Hude I, Sasse S, Engert A, Bröckelmann PJ. The emerging role of immune checkpoint inhibition in malignant lymphoma. Haematologica. 2017;102(1):30–42. doi:10.3324/haematol.2016.150656.
   PubMed Web of Science ®Google Scholar
• Yang ZZ, Novak AJ, Stenson MJ, Witzig TE, Ansell SM. Intratumoral CD4+CD25+ regulatory T-cell-mediated suppression of infiltrating CD4+ T cells in B-cell non-Hodgkin lymphoma. Blood. 2006;107(9):3639–3646. doi:10.1182/blood-2005-08-3376.
   PubMed Web of Science ®Google Scholar
• Myklebust JH, Irish JM, Brody J, Czerwinski DK, Houot R, Kohrt HE, Timmerman J, Said J, Green MR, Delabie J. High PD-1 expression and suppressed cytokine signaling distinguish T cells infiltrating follicular lymphoma tumors from peripheral T cells. Blood. 2013;121(8):1367–1376. doi:10.1182/blood-2012-04-421826.
   PubMed Web of Science ®Google Scholar
• Carreras J, Lopez-Guillermo A, Roncador G, Villamor N, Colomo L, Martinez A, Hamoudi R, Howat WJ, Montserrat E, Campo E. High numbers of tumor-infiltrating programmed cell death 1-positive regulatory lymphocytes are associated with improved overall survival in follicular lymphoma. J Clin Oncol. 2009;27(9):1470–1476. doi:10.1200/JCO.2008.18.0513.
   PubMed Web of Science ®Google Scholar
• Xu-Monette ZY, Zhou J, Young KH. PD-1 expression and clinical PD-1 blockade in B-cell lymphomas. Blood. 2018;131(1):68–83. doi:10.1182/blood-2017-07-740993.
   PubMed Web of Science ®Google Scholar
• Capietto AH, Martinet L, Fournié JJ. How tumors might withstand γδ T cell attack. Cell Mol Life Sci. 2011;68(14):2433–2442. doi:10.1007/s00018-010-0573-6.
   PubMed Web of Science ®Google Scholar
• Capietto AH, Martinet L, Fournie JJ. Stimulated gammadelta T cells increase the in vivo efficacy of trastuzumab in HER-2+ breast cancer. J Immunol. 2011;187(2):1031–1038. doi:10.4049/jimmunol.1100681.
   PubMed Web of Science ®Google Scholar
• Fournié JJ, Sicard H, Poupot M, Bezombes C, Blanc A, Romagné F, Ysebaert L, Laurent G. What lessons can be learned from γδ T cell-based cancer immunotherapy trials? Cell Mol Immunol. 2013;10(1):35–41. doi:10.1038/cmi.2012.39.
   PubMed Web of Science ®Google Scholar
• Meraviglia S, Lo Presti E, Dieli F, Stassi G. γδ T cell-based anticancer immunotherapy: progress and possibilities. Immunotherapy. 2015;7(9):949–951. doi:10.2217/imt.15.68.
   PubMed Web of Science ®Google Scholar
• Silva-Santos B, Serre K, Norell H. γδ T cells in cancer. Nat Rev Immunol. 2015;15(11):683–691. doi:10.1038/nri3904.
   PubMed Web of Science ®Google Scholar
• Gertner-Dardenne J, Bonnafous C, Bezombes C, Capietto AH, Scaglione V, Ingoure S, Cendron D, Gross E, Lepage JF, Quillet-Mary A, et al. Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytotoxicity induced by therapeutic antibodies. Blood.2009;113(20):4875–4884. doi:10.1182/blood-2008-03-146472.
   PubMed Web of Science ®Google Scholar
• Sicard H, Al Saati T, Delsol G, Fournié JJ. Synthetic phosphoantigens enhance human Vgamma9Vdelta2 T lymphocytes killing of non-Hodgkin’s B lymphoma. Mol Med. 2001;7(10):711–722.
   PubMed Web of Science ®Google Scholar
• Rossi J-F, Solal-Celigny P, Soubeyran P. Phase I/II study IPH101, gamma delta T cell agonist, in combination with rituximab re-treatment in patients with low grade follicular lymphoma. EHA Meeting; 2010. Abstract 1101.
   Google Scholar
• Musso A, Catellani S, Canevali P, Tavella S, Venè R, Boero S, Pierri I, Gobbi M, Kunkl A, Ravetti JL, et al. Aminobisphosphonates prevent the inhibitory effects exerted by lymph node stromal cells on anti-tumor Vδ 2 T lymphocytes in non-Hodgkin lymphomas. Haematol.2014;99(1):131–139. doi:10.3324/haematol.2013.097311.
   PubMed Web of Science ®Google Scholar
• Braza MS, Klein B, Fiol G, Rossi JF. γδ T-cell killing of primary follicular lymphoma cells is dramatically potentiated by GA101, a type II glycoengineered anti-CD20 monoclonal antibody. Haematologica. 2011;96(3):400–407. doi:10.3324/haematol.2010.029520.
   PubMed Web of Science ®Google Scholar
• Iwasaki M, Tanaka Y, Kobayashi H, Murata-Hirai K, Miyabe H, Sugie T, Toi M, Minato N. Expression and function of PD-1 in human γδ T cells that recognize phosphoantigens. Eur J Immunol. 2011;41(2):345–355. doi:10.1002/eji.201040959.
   PubMed Web of Science ®Google Scholar
• Decaup E, Jean C, Laurent C, Gravelle P, Fruchon S, Capilla F, Al Saati T, Frenois FX, Laurent G, Klein C, et al. Anti-tumor activity of obinutuzumab and rituximab in a follicular lymphoma 3D model. Blood Cancer J. 2013;3:e131. doi:10.1038/bcj.2013.32.
   PubMed Web of Science ®Google Scholar
• Gravelle P, Jean C, Valleron W, Laurent G, Fournié JJ. Innate predisposition to immune escape in follicular lymphoma cells. Oncoimmunol. 2012;1(4):555–556. doi:10.4161/onci.19365.
   PubMed Web of Science ®Google Scholar
• Gravelle P, Jean C, Familiades J, Decaup E, Blanc A, Bezombes-Cagnac C, Laurent C, Savina A, Fournié JJ, Laurent G. Cell growth in aggregates determines gene expression, proliferation, survival, chemoresistance, and sensitivity to immune effectors in follicular lymphoma. Am J Pathol. 2014;184(1):282–295. doi:10.1016/j.ajpath.2013.09.018.
   PubMed Web of Science ®Google Scholar
• Mössner E, Brünker P, Moser S, Püntener U, Schmidt C, Herter S, Grau R, Gerdes C, Nopora A, van Puijenbroek E, et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell-mediated B-cell cytotoxicity. Blood.2010;115(22):4393–4402. doi:10.1182/blood-2009-06-225979.
   PubMed Web of Science ®Google Scholar
• Guo S, Chan JKC, Iqbal J, McKeithan T, Fu K, Meng B, Pan Y, Cheuk W, Luo D, Wang R, et al. EZH2 mutations in follicular lymphoma from different ethnic groups and associated gene expression alterations. Clin Cancer Res.2014;20(12):3078–3086. doi:10.1158/1078-0432.CCR-13-3045.
   PubMed Web of Science ®Google Scholar
• Green MR, Gentles AJ, Nair RV, Irish JM, Kihira S, Liu CL, Kela I, Hopmans ES, Myklebust JH, Ji H, et al. Hierarchy in somatic mutations arising during genomic evolution and progression of follicular lymphoma. Blood.2013;121(9):1604–1611. doi:10.1182/blood-2012-09-457283.
   PubMed Web of Science ®Google Scholar
• Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med.2015;21(8):938–945. doi:10.1038/nm.3909.
   PubMed Web of Science ®Google Scholar
• Tosolini M, Pont F, Poupot M, Vergez F, Nicolau-Travers ML, Vermijlen D, Sarry JE, Dieli F, Fournié JJ. Assessment of tumor-infiltrating TCRVγ9Vδ2 γδ lymphocyte abundance by deconvolution of human cancers microarrays. Oncoimmunology. 2017;6(3):e1284723. doi:10.1080/2162402X.2017.1284723.
   PubMed Web of Science ®Google Scholar
• Poccia F, Cipriani B, Vendetti S, Colizzi V, Poquet Y, Battistini L, López-Botet M, Fournié JJ, Gougeon ML. CD94/NKG2 inhibitory receptor complex modulates both anti-viral and anti-tumoral responses of polyclonal phosphoantigen-reactive V gamma 9V delta 2 T lymphocytes. J Immunol. 1997;159(12):6009–6017.
   PubMed Web of Science ®Google Scholar
• Poupot M, Pont F, Fournié JJ. Profiling blood lymphocyte interactions with cancer cells uncovers the innate reactivity of human gamma delta T cells to anaplastic large cell lymphoma. J Immunol. 2005;174(3):1717–1722.
   PubMed Web of Science ®Google Scholar
• Gertner J, Wiedemann A, Poupot M, Fournié JJ. Human gammadelta T lymphocytes strip and kill tumor cells simultaneously. Immunol Lett. 2007;110(1):42–53. doi:10.1016/j.imlet.2007.03.002.
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–264. doi:10.1038/nrc3239.
   PubMed Web of Science ®Google Scholar
• Purwada A, Singh A. Immuno-engineered organoids for regulating the kinetics of B-cell development and antibody production. Nat Protoc. 2017;12(1):168–182. doi:10.1038/nprot.2016.157.
   PubMed Web of Science ®Google Scholar
• Mannino RG, Santiago-Miranda AN, Pradhan P, Qiu Y, Mejias JC, Neelapu SS, Roy K, Lam WA. 3D microvascular model recapitulates the diffuse large B-cell lymphoma tumor microenvironment in vitro. Lab Chip. 2017;17(3):407–414. doi:10.1039/c6lc01204c.
   PubMed Web of Science ®Google Scholar
• Amé-Thomas P, Tarte K. The yin and the yang of follicular lymphoma cell niches: role of microenvironment heterogeneity and plasticity. Semin Cancer Biol. 2014;24:23–32. doi:10.1016/j.semcancer.2013.08.001.
   PubMed Web of Science ®Google Scholar
• Huang Y, Chen Z, Jang JH, Baig MS, Bertolet G, Schroeder C, Huang S, Hu Q, Zhao Y, Lewis DE, et al. PD-1 blocks lytic granule polarization with concomitant impairment of integrin outside-in signaling in the natural killer cell immunological synapse. J Allergy Clin Immunol. 2018;142(4):1311–1321. doi:10.1016/j.jaci.2018.02.050.
   PubMed Web of Science ®Google Scholar
• Daydé D, Ternant D, Ohresser M, Lerondel S, Pesnel S, Watier H, Le Pape A, Bardos P, Paintaud G, Cartron G. Tumor burden influences exposure and response to rituximab: pharmacokinetic-pharmacodynamic modeling using a syngeneic bioluminescent murine model expressing human CD20. Blood. 2009;113(16):3765–3772. doi:10.1182/blood-2008-08-175125.
   PubMed Web of Science ®Google Scholar
• Lesokhin AM, Ansell SM, Armand P, Scott EC, Halwani A, Gutierrez M, Millenson MM, Cohen AD, Schuster SJ, Lebovic D, et al. Nivolumab in patients with relapsed or refractory hematologic malignancy: preliminary results of a phase Ib study. J Clin Oncol.2016;34(23):2698–2704. doi:10.1200/JCO.2015.65.9789.
   PubMed Web of Science ®Google Scholar
• Westin JR, Chu F, Zhang M, Fayad LE, Kwak LW, Fowler N, Romaguera J, Hagemeister F, Fanale M, Samaniego F, et al. Safety and activity of PD-1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial. Lancet Oncol.2014;15(1):69–77. doi:10.1016/S1470-2045(13)70510-2.
   PubMed Web of Science ®Google Scholar
• Nastoupil LJ, Westin JR, Fowler NH, Fanale MA, Samaniego F, Oki Y, Obi C, Cheng JX, Ma MCJ, Wang Z, et al. High response rates with pembrolizumab in combination with rituximab in patients with relapsed follicular lymphoma: interim results of an on open-label, phase II study. Hematol Oncol. 35(S2):120–121. doi:10.1002/hon.2437_108.
   Google Scholar
• Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, Advani R, Ghielmini M, Salles GA, Zelenetz AD, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood.2016;127(20):2375–2390. doi:10.1182/blood-2016-01-643569.
   PubMed Web of Science ®Google Scholar
• Buades A, Coll B, Morel JM. A non-local algorithm for image denoising. IEEE. 2005;2:60–65.
   Google Scholar
• Edgar R, Domrachev M, Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1):207–210. doi:10.1093/nar/30.1.207.
   PubMed Web of Science ®Google Scholar
• Brodtkorb M, Lingjærde OC, Huse K, Trøen G, Hystad M, Hilden VI, Myklebust JH, Leich E, Rosenwald A, Delabie J, et al. Whole-genome integrative analysis reveals expression signatures predicting transformation in follicular lymphoma. Blood. 2014;123(7):1051–1054. doi:10.1182/blood-2013-07-512392.
   PubMed Web of Science ®Google Scholar
• Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12(5):453–457. doi:10.1038/nmeth.3337.
   PubMed Web of Science ®Google Scholar
• Watkins AJ, Hamoudi RA, Zeng N, Yan Q, Huang Y, Liu H, Zhang J, Braggio E, Fonseca R, de Leval L, et al. An integrated genomic and expression analysis of 7q deletion in splenic marginal zone lymphoma. PLoS One. 2012;7(9):e44997. doi:10.1371/journal.pone.0044997.
   PubMed Web of Science ®Google Scholar